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Denitrification: from Genes to Ecosystems

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Denitrification: from Genes to Ecosystems Denitrification: From Genes to Ecosystems Christopher M. Jones Faculty of Natural Resources and Agricultural Sciences Department of Microbiology Uppsala Doctoral Thesis Swedish University of Agricultural Sciences Uppsala 2010 Acta Universitatis agriculturae Sueciae 2010:83 Cover: Montage showing the phylogeny of globally distributed nirS sequences, where tip labels indicate habitat type (see Figure 6, this thesis). Earth photo courtesy of NASA. ISSN 1652-6880 ISBN 978-91-576-7528-6 © 2010 Christopher M. Jones, Uppsala Print: SLU Service/Repro, Uppsala 2010 Denitrification: From Genes to Ecosystems Abstract Denitrification is a part of the global nitrogen cycle in which fixed nitrogen in the biosphere is returned to the atmosphere, and is mediated by diverse communities of microorganisms. This thesis seeks to gain a greater understanding of the ecology of denitrifying microorganisms by examining the pathway from four different aspects; gene, population, community, and ecosystem. A combination of bioinformatic analysis of denitrification genes in pure cultures and environmental samples as well as experimental work with denitrifying bacterial cultures and soil microcosms was performed to understand the relationship between genes and ecosystems in denitrification. Analysis of the phylogeny of genes involved in key steps in the denitrificaiton pathway revealed a different evolutionary pattern for each gene, as processes such as horizontal gene transfer, duplication/divergence, and lineage sorting have contributed differentially to the evolution of catalytic genes at each step. However, genetic variation is not easily translated into an extended phenotype for a population of denitrifiers, as the denitrification phenotype of a set of closely related denitrifying Bacillus soil isolates was variable depending on pH. Yet, the genetic community structure was shown to be an important factor in determining denitrification rates and end product ratios, as denitrifying communities in soil microcosms showed differential response to altered ratios of organisms with an without the ability to reduce nitrous oxide. Finally, patterns of nirS and nirK sequences suggested that community assembly of both denitrifier types was largely driven by niche-based processes, as community structure varied among habitats with different salinities. However, nirS and nirK denitrifiers were not ecologically equivalent, as patterns of phylogenetic clustering among co-existing nirS and nirK type denitrifying communities along the same environmental gradient were not comparable. In conclusion, denitrification is a complex ecological function that is regulated by the interaction between gene and environmental factors, and evolutionary processes that underlying the diversification and distribution of denitrification genes may have direct consequences on the denitrification unction in ecosystems. Keywords: denitrification, phylogeny, microevolution, community assembly, niche, nirK, nirS, nosZ, Bacillus, phenotype Author’s address: Christopher M. Jones, SLU, Department of Microbiology, P.O. Box 7025, 750-07 Uppsala, Sweden E-mail: [email protected] Dedication To my family, on both sides of the Atlantic… Contents Denitrification: From Genes to Ecosystems 1 List of Publications 7 Abbreviations 9 1 Introduction 11 1.1 Denitrification in terrestrial and aquatic ecosystems 11 1.2 The Denitrification Pathway 13 1.3 Evolutionary aspects of Denitrification 14 1.4 Community and Functional Ecology of Denitrifiers 16 1.5 Aim and Outline of Thesis 17 2 Evolutionary influences on the denitrification Pathway 21 2.1 Diverging evolutionary histories of nitrogen cycling genes 21 2.2 Phylogeny estimation and hypothesis testing – likelihood and Bayesian techniques 22 2.2.1 Sequence Alignment 22 2.2.2 Phylogenetic Analysis using Maximum Likelihood 24 2.2.3 Genomic Signatures – GC content and Codon usage 26 2.3 Modular evolution of the denitrification pathway 27 2.4 Future Directions 31 3 Denitrifier Diversity at the population level - physiological vs. genetic diversity 33 3.1 Population – the unit of evolution 33 3.2 Microvariation in Populations 34 3.3 Genetic and Phenotypic Characterization of Cultivated Denitrifiers 35 3.3.1 Culture based studies 35 3.3.2 Genetic Characterization 36 3.4 Potential Importance of Microvariation 37 3.5 Future directions 38 4 Denitrification response to altered community structure 41 4.1 Does Structure Matter? 41 4.2 Microcosms – linking denitrifier function and community structure. 43 4.3 Importance of community structure 44 4.4 Future directions – Observation vs. Manipulation 45 5 Global Patterns of Denitrifier Diversity 47 5.1 Shaping Denitrifier Community Structure 47 5.2 Phyloecology - Merging of Ecology and Evolution 49 5.3 Influence of habitat on denitrifier communities. 51 5.4 Future Directions 54 6 Conclusions and Perspectives 55 References 59 Acknowledgements 73 List of Publications I Jones CM, Stres B, Rosenquist M, Hallin S. (2008). Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Molecular Biology and Evolution 25 (9), 1955-1966. II Jones, CM, Welsh AW, Throbäck I, Dörsch P, Bakken LR, Hallin S. Phenotypic and genotypic heterogeneity among closely related soil- borne denitrifying Bacillus isolates harbouring the nosZ gene. Manuscript. III Philippot L, Andert J, Jones CM, Bru D, Hallin S (2010). Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Global Change Biology DOI: 10.1111/j.1365- 2486.2010.02334.x IV Jones CM, Hallin S (2010). Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. The ISME Journal 4, 633-641. Papers I, III and IV are reproduced with the permission of the publishers. 7 The contribution of the author to the papers included in this thesis was as follows: I Performed a major part of the data collection, phylogenetic analysis, and writing of the manuscript. II Performed a major part of the laboratory work, phylogenetic and clustering analysis, and writing of the manuscript. III Participated in the planning of the experiment, performed the statistical analysis, and a minor part of the lab work and writing of the manuscript. IV Participated in the planning of the study, performed all data collection, analysis, and a major part of the writing of the manuscript. In addition to the papers within this thesis, the author has contributed to the following papers within the timeframe of the thesis work: Hallin S., Jones, C.M., Schloter, M. and Philippot, L. 2009. Relationship between N-cycling communities and ecosystem functioning in a 50-year- old fertilization experiment. The ISME Journal 3, 597-605. Beier, S., Jones, C. M., Mohit, V., Hallin, S. and Bertilsson, S. Global phylogeography of chitinase genes in aquatic metagenomes. Manuscript. Willing B., Vörös A., Roos S., Jones C., Jansson A. and Lindberg J.E. 2009. Changes in faecal bacteria associated with concentrate and forage-only diets fed to horses in training. Equine Veterinary Journal 41(9), 908-914. 8 Abbreviations AFLP Amplified fragment length polymorphism cnorB Gene encoding cytochrome-c nitric oxide reductase variant nirK Gene encoding copper nitrite reductase nirS Gene encoding cytochrome-cd1 nitrite reductase NMS Non-metric multidimensional scaling - NO3 Nitrate - NO2 Nitrite NO Nitric oxide N2O Nitrous Oxide N2 Dinitrogen gas nosZ Gene encoding nitrous oxide reductase NRI Net relatedness index NTI Nearest taxa index qnorB Gene encoding quinol nitric oxide reductase UniFrac Unique Fraction Index 9 10 1 Introduction Denitrification is a facultative respiratory pathway during which nitrate - (NO3 ) is stepwise reduced to nitrous oxide (N2O) or nitrogen gas (N2) via - nitrite (NO2 ) and nitric oxide (NO) under oxygen-limited conditions. Each step is coupled to the electron transport chain such that electrons from reductants can be passed on to different nitrogen oxides, allowing for the generation of a proton gradient across the membrane for energy conservation. On the ecosystem scale, denitrification effectively closes the nitrogen cycle by converting soluble nitrogen to N2, which is returned to the atmosphere and once again made available for nitrogen fixation. Because of its role in regulating nitrogen in ecosystems, the ecology of denitrification has been the topic of innumerable studies. This interest will only continue to grow given the recent concerns over the effect of N2O emissions from different environments on climate change, as N2O is both a potent greenhouse gas and a cause of stratospheric ozone depletion. 1.1 Denitrification in terrestrial and aquatic ecosystems The global nitrogen cycle begins with the fixation of atmospheric nitrogen + into ammonium (NH4 ) through physical, anthropogenic, or microbially + mediated processes. The NH4 that is not incorporated into growing plant - or microbial biomass can be converted to NO3 via nitrification, an aerobic process, or respired to N2 through anaerobic ammonia oxidation (ANAMMOX). The nitrate produced by nitrification is then used in denitrification, which in addition to ANAMMOX is a major pathway by which fixed nitrogen is returned to the atmosphere. Denitrification can - - result from chemical reactions of NO3 /NO2 with metal cations at low pH conditions (Van Cleemput, 1998); however the bulk of denitrification 11 activity in most ecosystems is mediated by heterotrophic bacteria and archaea. Denitrifying
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